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most such deaths are attributable to preterm birth or TABLE 1. Causes of Postneonatal Death in the 1988 NMIHS
congenital anomalies; we also excluded deaths from (Excluding Malignancy and Congenital Anomalies)
congenital anomaly or malignancy occurring in the Postneonatal Death Causes and ICD-9 Codes n
postneonatal period. Infections (n 255)
001–139 Infectious and parasitic diseases 47
METHODS 240–279 Endocrine, nutritional, and metabolic 1
Subjects diseases and immunity disorders
The 1988 NMIHS is a nationally representative stratified sys- 320–389 Meningitis and other diseases of the 56
tematic sample of 9953 women who had live births, 3309 who had nervous system and sense organs
late fetal deaths (28 weeks’ gestation or more, including term 460–519 Diseases of the respiratory system 124
stillborn), and 5332 who had infant deaths (a liveborn child who 520–579 Diseases of the digestive system 27
died by 1 year of age) in 1988.22 These live births and infant deaths Injuries (n 126)
were from 48 states (none from Montana or South Dakota), the E800–E999 Injury and poisoning 126
District of Columbia, and New York City. Black infants were SIDS (n 591)
oversampled in all 3 components of the NMIHS, and very low 798.0 Sudden infant death syndrome 591
birth weight ( 1500 g) and moderately low birth weight (1500 – Others and unknown (n 232)
2499 g) infants were oversampled in the live birth component. 280–289 Diseases of the blood and blood- 3
Vital events to unmarried mothers in Arizona, Kansas, and North forming organs
Dakota were excluded.22 Only live births and infant deaths are 760–779 Certain conditions originating in the 30
included in our analysis. The final sample for analysis, containing perinatal period
1204 postneonatal deaths (cases) and 7740 live births (still alive 780–797, 798.1–799 Symptoms, signs, and all 87
and 1 year old at survey; controls), is shown in Fig 1. other ill-defined conditions
Mothers answered a mailed questionnaire on characteristics of Unknown 112
the parents, previous and subsequent pregnancies, prenatal care ICD-9 indicates International Classification of Diseases, Ninth
and health habits, and the infant’s health. Information from the Revision.
birth certificate and death certificate was also included in the data
set. Women whose infant died before 1 month or did not live with
her at any time after birth were not asked the breastfeeding reported at birth, live birth order, and single or multiple birth. The
questions. The answer “yes” or “no” to the question, “Did you race- and birth weight–specific analyses did not include race or
ever breastfeed this infant?” was defined as “ever breastfed” or birth weight terms. We also did proportional hazard models to
“never breastfed” in the analysis. The duration of breastfeeding is calculate the hazard ratio for ever breastfeeding in cases only to
from the answer to the question, “How old was your infant when determine whether breastfeeding delayed death even among in-
you stopped breastfeeding?” fants who died.
Causes of postneonatal death (International Classification of Dis- We were interested in determining whether prolonged breast-
eases, Ninth Revision) were obtained from death certificates. For feeding had greater effects. Because these are case-control data,
some analyses, we divided the deaths into 4 categories: infections, however, we cannot simply put breastfeeding duration in the
injuries, SIDS, and others (Table 1). logistic model, because the opportunity for the case infants to
breastfeed extends only to their age at death, whereas the controls
Statistics can breastfeed for up to 1 year. So, unless the case infants died
We used logistic regression to calculate the odds ratio (OR) of very late in the infancy (clearly not true in this study), their
ever having breastfed to never having breastfed for postneonatal opportunity for prolonged breastfeeding was significantly com-
death. We first considered all postneonatal deaths as cases and the promised. We addressed this problem by doing an analysis using
live births as controls. We then duplicated the analysis using cases the model described above but limiting the case group to those
from each of 4 cause-of-death categories, whereas the controls who had survived 3 months or more and using 3 months of
remained unchanged. Race and birth weight are so strongly re- breastfeeding versus 3 months or none in place of the ever/
lated to breastfeeding that we did analyses separately by race and never breastfed variable. This equalizes the opportunity to breast-
birth weight category. Covariates included mother’s age, educa- feed at 3 months in the cases and controls, at a cost of reduced
tion, smoking during pregnancy, and participation in the federal sample size among the cases. We then can compare the OR of ever
nutritional support program for Women, Infants, and Children; breastfeeding with the OR of breastfeeding for 3 months or more.
and infant’s gender, race, birth weight, congenital malformation We used SAS 8.2 (SAS, Inc, Cary, NC) for preliminary tabula-
Fig 1. Samples for analysis from the
1988 National Maternal and Infant Sur-
vey. Of 449 subjects without breastfeed-
ing information in infant death group,
323 answered “No” to the question,
“Was the baby at home with mother at
any time after delivery?”, 78 had no
available answer, and another 48 an-
swered “Yes” but did not provide in-
formation regarding breastfeeding. Of
198 subjects without breastfeeding in-
formation in the live birth group, 100
answered “No” to the question, 37 had
no available answer, and another 61 an-
swered “Yes” but did not provide in-
formation regarding breastfeeding.
N/A denotes not available.
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4.
tion and descriptive analysis and, because of the oversampling of
black and low birth weight infants, SUDAAN 8.0.2 (Research
Triangle Institute, Research Triangle Park, NC) to reweight the
sample for the overall estimates and to calculate the ORs and 95%
confidence intervals (CIs) in the final models. SUDAAN adjust-
ment gives an estimate of the number of people in the US popu-
lation with a given characteristic in that year; it uses different
weights depending on the degree to which a given group was
oversampled by design. For example, on the basis of the sampling
frequencies, the sample of 7740 live births represents 3 186 497 live
births in 1988, and the sample of 1204 postneonatal deaths repre-
sents 9145 deaths as a result of causes other than malignancy or
congenital anomaly.
RESULTS
As seen in Table 2, after adjustment with
SUDAAN, cases and controls differ on all covari-
ables of interest. Mothers of the children who died
are younger, are less educated, and smoke more
often during pregnancy. The children who died had Fig 2. Age at death for postneonatal deaths.
a higher birth order and were more often male, black,
and of low birth weight. There remained an excess of
children with congenital anomalies among the cases, marginally lower in the ever breastfed infants (haz-
although children who died by 28 days or who died ard ratio: 0.91; 95% CI: 0.79 –1.06).
of their congenital anomaly or a malignant tumor In addition to the covariates adjusted in the mod-
were excluded. Age at death is shown in Fig 2. Most els, we examined possible confounding from cesar-
children who died did so before they had completed ean section. We found no difference in SUDAAN
4 months of life. adjusted proportion of cesarean section between
After adjustment for sampling strategy with cases (20.2%) and controls (18.3%). Cesarean section
SUDAAN, 53% of control infants were ever breast- did not affect the percentage of ever breastfeeding in
fed, compared with 38% of cases. Logistic regression either cases or controls and had no effect on the
models showed an OR of 0.79 (95% CI: 0.67– 0.93) for estimate of the strength of the effect of breastfeeding
ever breastfed (Table 3). Race-specific analyses gave when it was included in the models. For duration of
similar estimates for the OR, although the proportion breastfeeding, comparing cases who survived 3
ever breastfed was much lower in black infants. For months (n 691 in original sample and n 5363
the low birth weight infants, the OR of ever breastfed after adjustment with SUDAAN) and all controls, 3
was 0.97 (95% CI: 0.64 –1.47). The estimates from months or more of breastfeeding showed an OR of
logistic models changed only slightly by category of 0.62 (95% CI: 0.46 – 0.82), less (ie, more protective)
cause of death (Table 3). The overall risk estimate than the OR for ever/never breastfed (0.79; 95% CI:
changes little even when we include deaths as a 0.67– 0.93).
result of an underlying congenital anomaly (n 212)
or malignant tumor (n 10); the OR for overall DISCUSSION
postneonatal death was 0.74 (95% CI: 0.63– 0.87). Breastfed children have a decreased risk of post-
Among cases only, a proportional hazard model neonatal death in the United States, although infec-
showed that the risk of death at any specific time was tious diseases, those most plausibly prevented by
TABLE 2. Characteristics of Case (Postneonatal Death) and Control (Live Birth) infants
Variables Original Samples SUDAAN-Adjusted
Live Birth Postneonatal Live Birth Postneonatal
(n 7740) Death (n 1204) (N 3186497) Death (N 9145)
Mother’s age (y; mean SEM)* 25.6 0.06 23.9 0.2 26.3 0.02 24.4 0.2
Mother’s education (y; mean SEM)* 12.3 0.03 11.7 0.1 12.6 0.04 11.8 0.1
Male gender* 50.3 59.8 52.0 59.2
Race*
White 44.4 50.0 77.2 68.3
Black 52.2 46.6 17.2 27.3
Others 3.4 3.4 5.5 4.4
Live birth order*
1 40.7 30.8 41.7 32.1
2 30.9 32.3 32.8 32.5
3 28.4 36.9 25.5 35.4
Plurality single* 95.2 95.0 98.0 95.4
Birth weight 2500 g* 26.0 23.8 13.0 21.9
Congenital malformation reported at birth* 1.2 2.8 0.8 2.9
Maternal smoking during pregnancy* 22.9 38.6 21.7 39.8
WIC after delivery* 50.2 55.7 36.8 49.2
n indicates sample size; N, US population estimate; SEM, standard error of the mean; WIC, the nutrition program for Women, Infants, and
Children.
* P .01 (SUDAAN-adjusted).
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5.
TABLE 3. Percentage of Ever Breastfed and ORs for Postneonatal Deaths
Original Samples SUDAAN-Adjusted
Live births Postneonatal Adjusted* OR Live Births Postneonatal Adjusted* OR
Deaths (95% CI) Deaths (95% CI)
n % Ever n % Ever Ever/Never N % Ever N % Ever Ever/never
Breastfed Breastfed Breastfed Breastfed Breastfed Breastfed
Total 7740 39.7 1204 31.2 0.76 (0.65–0.88) 3 186 497 53.4 9145 37.7 0.79 (0.67–0.93)
Race specific
Black 4038 26.0 561 16.0 0.67 (0.52–0.87) 549 360 27.9 2498 16.8 0.69 (0.53–0.90)
Nonblack 3702 54.7 643 44.3 0.79 (0.65–0.96) 2 637 137 58.7 6647 45.6 0.81 (0.66–0.98)
Birth weight specific
2500 g 2015 27.7 287 24.7 0.87 (0.60–1.37) 200 443 36.1 2002 31.4 0.97 (0.64–1.47)
2500 g 5725 43.9 917 33.2 0.73 (0.61–0.86) 2 986 054 54.5 7143 39.5 0.76 (0.64–0.91)
Death cause specific
Infections - - 255 30.2 0.75 (0.55–1.02) - - 1914 37.0 0.76 (0.54–1.07)
Injuries - - 126 28.6 0.67 (0.43–1.05) - - 971 31.9 0.59 (0.38–0.94)
SIDS - - 591 31.6 0.77 (0.63–0.95) - - 4514 38.3 0.84 (0.67–1.05)
Others - - 232 32.3 0.76 (0.54–1.07) - - 1745 40.4 0.81 (0.56–1.16)
* Adjusted for mother’s age, education, and smoking during pregnancy and infant’s gender, race (except for race subgroup analyses), birth
weight (except for birth weight subgroup analyses), congenital malformation reported at birth, live birth order, plurality, and WIC status.
breastfeeding, no longer contribute substantially to physical proximity, it deserves additional study,
postneonatal mortality. Longer breastfeeding was as- having been seen both in his data and in ours.
sociated with lower risk of postneonatal death. There To some extent, the policy implications of demon-
is little heterogeneity of this effect among the differ- strating benefits of breastfeeding depend on whether
ent causes of death, at least with the coarse group- the benefits will be achieved by persuading a mother
ings that we used. Even among cases only, those who to breastfeed when she otherwise might not have.
were ever breastfed live marginally longer. This is a Strictly, though, causality is difficult to demonstrate
very large data set, representative of the US popula- for any specific part of the interaction between the
tion, albeit in 1988. Because postneonatal mortality in breastfeeding mother and her child. It may be that
the United States has declined from 3.6/1000 in 1986 breastfeeding represents a package of skills, abilities,
to 2.3/1000 in 2000, a prospective study now would and emotional attachments that mark families whose
need to enroll 60 000 newborns and follow them for infants survive and that it is these factors that pro-
1 year to approach the power and precision of these duce the benefits seen, rather than breastfeeding or
data. Familiar confounders can be accounted for in breast milk per se. We cannot randomize breastfeed-
the analysis, and the oversampling among black in- ing, although it is possible to randomize breast milk:
fants and premature infants allows reasonably pre- Lucas et al23 conducted an ingenious study in which
cise and robust estimates for them specifically. We premature infants who were fed their mother’s milk
see a more modest benefit than Forste, who observed from a bottle did better on follow-up testing than
a remarkably strong protective OR of 0.2 in a model children who were fed formula.
with only race, birth weight, and breastfeeding. We Reverse causality, produced by the motivation or
examined the 1995 National Survey of Family enthusiasm that marks a healthier child who can
Growth data, which formed half of the basis of the breastfeed or by specific characteristics of the child’s
Forste analysis (1988 and 1995). An estimate adjust- illness, such as cleft palate and breathlessness during
ing for most covariables used in our study gives an sucking, that prevent breastfeeding might produce
OR of 0.7 for breastfeeding and all-cause postneo- an artificial benefit of breastfeeding. Eliminating
natal mortality, comparable to our estimate in this deaths in the first month and deaths from congenital
study. Carpenter did not give an OR for his UK anomaly or malignant tumor, where infants who are
study, but it is possible to estimate an OR of 0.4 from unable to breastfeed are concentrated, and using the
the published data. Because Carpenter used a set of initial feeding method to categorize feeding should
causes of death (what he termed “preventable diminish but perhaps not eliminate this problem.
death”) that are not readily extractable from Interna- However, excluding these deaths also excludes the
tional Classification of Diseases, Ninth Revision coded chance to examine whether breastfeeding has any
death certificates and deaths out to 2 years of age, we effects on these deaths, especially those who are not
cannot compare our estimate directly with his. fatally ill at birth. In a prospective study, it might be
Is it plausible that breastfeeding protects not only possible to include neonatal deaths if careful atten-
against infectious disease mortality, through familiar tion were paid to the reason that a child was breast-
immune enhancing mechanisms, but also against fed or not. We do not have such data; however, we
SIDS, accidental death, and others? Although a sat- can eliminate from the analysis any child, case or
isfactory mechanism has not yet been proposed, the control, who was admitted to the neonatal intensive
protection from SIDS has been seen in several studies care unit. This yields a similar but less precisely
and is under investigation. For accidental death, Car- estimated OR of 0.83 (95% CI: 0.67–1.03).
penter also observed lower risk, and although the The NMIHS data are from cases and controls and
association may represent something as simple as depend on interviews done after the child had sur-
e438 BREASTFEEDING AND RISK OF POSTNEONATAL DEATH
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ACKNOWLEDGMENTS
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We thank the National Center for Health Statistics at the Cen- 23. Lucas A, Morley R, Cole TJ, Lister G, Leeson-Payne C. Breast milk and
ters for Disease Control and Prevention for providing the 1988 subsequent intelligence quotient in children born preterm. Lancet. 1992;
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University of North Carolina at Chapel Hill for comments on 24. Kleinman JC, Kiely JL. Postneonatal mortality in the United States: an
statistical analysis and Drs Allen J. Wilcox and David M. Umbach international perspective. Pediatrics. 1990;86:1091–1097
at the National Institute of Environmental Health Sciences for 25. Ryan AS, Wenjun Z, Acosta A. Breastfeeding continues to increase into
comments on an earlier version of the manuscript. the new millennium. Pediatrics. 2002;110:1103–1109
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7.
Breastfeeding and the Risk of Postneonatal Death in the United States
Aimin Chen and Walter J. Rogan
Pediatrics 2004;113;e435-e439
DOI: 10.1542/peds.113.5.e435
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